Cryptosporidiosis: Host immune responses and the prospects for effective immunotherapies

Expert Review of Anti-Infective Therapy

Volumn 9, Issue 11, 2011, Pages 1077-1086

  McDonald, Vincent ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

adaptive immunity; antibodies; B cells; Cryptosporidium; host immunity; innate immunity; T cells; vaccines

Indexed keywords

GAMMA INTERFERON; MONOCLONAL ANTIBODY;

ANTIBODY SPECIFICITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COLOSTRUM; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; CYTOKINE RESPONSE; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPROMISED PATIENT; IMMUNOTHERAPY; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; LYMPHOCYTE FUNCTION; NATURAL KILLER CELL; NONHUMAN; PASSIVE IMMUNIZATION; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, PROTOZOAN; B-LYMPHOCYTES; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; CYTOKINES; DIARRHEA; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; IMMUNOCOMPROMISED HOST; IMMUNOTHERAPY; INTESTINES; KILLER CELLS, NATURAL; PROTOZOAN VACCINES; T-LYMPHOCYTES;

EID: 80155177956     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.11.123     Document Type: Review

References (105)

1. Davies AP, Chalmers RM. Cryptosporidiosis. BMJ 339, b4168 (2009).
2. Smith HV, Nichols RA, Mallon M et al. Natural Cryptosporidium hominis infections in Scottish cattle. Vet. Rec. 156, 710-711 (2005).
3. Current WL, Reese NC. A comparison of endogenous development of three isolates of Cryptosporidium in suckling mice. J. Protozool. 33, 98-108 (1986).
4. Chen XM, Keithly JS, Paya CV, LaRusso NF. Cryptosporidiosis. N. Engl. J. Med. 346, 1723-1731 (2002).
5. Amadi B, Mwiya M, Sianongo S et al. High dose prolonged treatment with nitazoxanide is not effective for cryptosporidiosis in HIV positive Zambian children: a randomised controlled trial. BMC Infect. Dis. 9, 195 (2009).
6. Macdonald TT, Monteleone I, Fantini MC, Monteleone G. Regulation of homeostasis and inflammation in the intestine. Gastroenterology 140, 1768-1775 (2011).
7. Mowatt AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3, 331-341 (2003).
8. Wells JM, Rossi O, Meijerink M, van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc. Natl Acad. Sci. USA 108(Suppl. 1), 4607-4614 (2011).
9. + T cells to proliferate and secrete interferon-γ. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1630-G1640 (2007).
10. + T lymphocytes synergize with murine intestinal epithelial cells to enhance proinflammatory response against an intracellular pathogen. J. Immunol. 168, 2988-2996 (2002).
11. Rescigno M. Dendritic cells in bacteria handling in the gut. J. Leukoc. Biol. DOI: 10.1189/jlb.0311141 (2011) (Epub ahead of print).
12. Brandtzaeg P. Mucosal immunity: induction, dissemination, and effector functions. Scand. J. Immunol. 70, 505-515 (2009).
13. Marcial MA, Madara JL. Cryptosporidium: cellular localization, structural analysis of absorptive cell-parasite membrane- membrane interactions in guinea pigs, and suggestion of protozoan transport by M cells. Gastroenterology 90, 583-594 (1986).
14. Laurent F, Eckmann L, Savidge TC et al. Cryptosporidium parvum infection of human intestinal epithelial cells induces polarized secretion of C-X-C chemokines. Infect. Immun. 65, 5067-5073 (1997).
15. Chen XM, Levine SA, Splinter PL et al. Cryptosporidium parvum activates nuclear factor kB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 120, 1774-1783 (2001).
16. Zaalouk TK, Bajaj-Elliott M, George JT, McDonald V. Differential regulation of β-defensin gene expression during Cryptosporidium parvum infection. Infect. Immun. 72, 2772-2779 (2004).
17. Auray G, Lacroix-Lamande S, Mancassola R, Dimier-Poisson I, Laurent F. Involvement of intestinal epithelial cells in dendritic cell recruitment during Cryptosporidium parvum infection. Microbes Infect. 9, 574-582 (2007).
18. Chen XM, O'Hara SP, Nelson JB et al. Multiple TLRs are expressed in human cholangiocytes and mediate host epithelial defense responses to Cryptosporidium parvum via activation of NF-kB. J. Immunol. 175, 7447-7456 (2005).
19. O'Hara SP, Chen XM. The cell biology of Cryptosporidium infection. Microbes Infect. 13, 721-730 (2011).
20. Yang YL, Buck GA, Widmer G. Cell sorting-assisted microarray profiling of host cell response to Cryptosporidium parvum infection. Infect. Immun. 78, 1040-1048 (2010).
21. Pollok RC, Farthing MJ, Bajaj-Elliott M, Sanderson IR, McDonald V. Interferon -γ induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 120, 99-107 (2001).
22. Choudhry N, Korbel DS, Edwards LA, Bajaj-Elliott M, McDonald V. Dysregulation of interferon-γ-mediated signalling pathway in intestinal epithelial cells by Cryptosporidium parvum infection. Cell Microbiol. 11, 1354-1364 (2009).
23. Heine J, Moon HW, Woodmansee DB. Persistent Cryptosporidium infection in congenitally athymic (nude) mice. Infect. Immun. 43, 856-859 (1984).
24. McDonald V, Deer R, Uni S, Iseki M, Bancroft GJ. Immune responses to Cryptosporidium muris and Cryptosporidium parvum in adult immunocompetent or immunocompromised (nude and SCID) mice. Infect. Immun. 60, 3325-3331 (1992).
25. Miller TA, Ware MW, Wymer LJ, Schaefer FW III. Chemically and genetically immunocompromised mice are not more susceptible than immunocompetent mice to infection with Cryptosporidium muris. Vet. Parasitol. 143, 99-105 (2007).
26. Kuhls TL, Mosier DA, Abrams VL, Crawford DL, Greenfield RA. Inability of interferon-γ and aminoguanidine to alter Cryptosporidium parvum infection in mice with severe combined immunodeficiency. J. Parasitol. 80, 480-485 (1994).
27. Barakat FM, McDonald V, Di Santo JP, Korbel DS. Roles for NK cells and an NK cell-independent source of intestinal γ interferon for innate immunity to Cryptosporidium parvum infection. Infect. Immun. 77, 5044-5049 (2009).
28. McDonald V, Robinson HA, Kelly JP, Bancroft GJ. Cryptosporidium muris in adult mice: adoptive transfer of immunity and protective roles of CD4 versus CD8 cells. Infect. Immun. 62, 2289-2294 (1994).
29. Tzipori S. Cryptosporidiosis in perspective. Adv. Parasitol. 27, 63-129 (1988).
30. Kutukculer N, Moratto D, Aydinok Y et al. Disseminated Cryptosporidium infection in an infant with hyper-IgM syndrome caused by CD40 deficiency. J. Pediatr. 142, 194-196 (2003).
31. Cosyns M, Tsirkin S, Jones M, Flavell R, Kikutani H, Hayward AR. Requirement of CD40-CD40 ligand interaction for elimination of Cryptosporidium parvum from mice. Infect. Immun. 66, 603-607 (1998).
32. Waters WR, Harp JA. Cryptosporidium parvum infection in T-cell receptor (TCR)-α- and TCR-δ-deficient mice. Infect. Immun. 64, 1854-1857 (1996).
33. Eichelberger MC, Suresh P, Rehg JE. Protection from Cryptosporidium parvum infection by γδ T cells in mice that lack αβ T cells. Comp Med. 50, 270-276 (2000).
34. Abrahamsen MS, Lancto CA, Walcheck B, Layton W, Jutila MA. Localization of αβ and γδ T lymphocytes in Cryptosporidium parvum-infected tissues in naive and immune calves. Infect. Immun. 65, 2428-2433 (1997).
35. Aguirre SA, Mason PH, Perryman LE. Susceptibility of major histocompatibility complex (MHC) class I- and MHC class II-deficient mice to Cryptosporidium parvum infection. Infect. Immun. 62, 697-699 (1994).
36. + T lymphocytes in protective immunity. J. Immunol. 147, 1014-1022 (1991).
37. + cells and -γ interferon in resolution of established Cryptosporidium parvum infection in mice. Infect. Immun. 61, 3928-3932 (1993).
38. Blanshard C, Jackson AM, Shanson DC, Francis N, Gazzard BG. Cryptosporidiosis in HIV-seropositive patients. QJ Med. 85, 813-823 (1992).
39. + T cells followed by clearance of intestinal cryptosporidiosis in an AIDS patient receiving highly active antiretroviral therapy. Gastroenterology 120, 984-987 (2001).
40. Singh I, Carville A, Tzipori S. Cryptosporidiosis in rhesus macaques challenged during acute and chronic phases of SIV infection. AIDS Res. Hum. Retroviruses 27(9), 989-997 (2011).
41. + cells in response to Cryptosporidium parvum antigen. J. Parasitol. 80, 67-72 (1994).
42. + intraepithelial lymphocytes. Infect. Immun. 64, 2556-2562 (1996).
43. Culshaw RJ, Bancroft GJ, McDonald V. Gut intraepithelial lymphocytes induce immunity against Cryptosporidium infection through a mechanism involving -γ interferon production. Infect. Immun. 65, 3074-3079 (1997).
44. Ungar BL, Burris JA, Quinn CA, Finkelman FD. New mouse models for chronic Cryptosporidium infection in immunodeficient hosts. Infect. Immun. 58, 961-969 (1990).
45. McDonald V, Bancroft GJ. Mechanisms of innate and acquired resistance to Cryptosporidium parvum infection in SCID mice. Parasite Immunol. 16, 315-320 (1994).
46. Leav BA, Yoshida M, Rogers K et al. An early intestinal mucosal source of -γ interferon is associated with resistance to and control of Cryptosporidium parvum infection in mice. Infect. Immun. 73, 8425-8428 (2005).
47. + T cells clear Cryptosporidium parvum from infected intestinal epithelial cells. Am. J. Trop. Med. Hyg. 82, 600-607 (2010).
48. Kirkpatrick BD, Haque R, Duggal P et al. Association between Cryptosporidium infection and human leukocyte antigen class I and class II alleles. J. Infect. Dis. 197, 474-478 (2008).
49. Kapel N, Benhamou Y, Buraud M, Magne D, Opolon P, Gobert JG. Kinetics of mucosal ileal γ-interferon response during cryptosporidiosis in immunocompetent neonatal mice. Parasitol. Res. 82, 664-667 (1996).
50. Fayer R, Gasbarre L, Pasquali P, Canals A, Almeria S, Zarlenga D. Cryptosporidium parvum infection in bovine neonates: dynamic clinical, parasitic and immunologic patterns. Int. J. Parasitol. 28, 49-56 (1998).
51. Wyatt CR, Brackett EJ, Savidge J. Evidence for the emergence of a type-1-like immune response in intestinal mucosa of calves recovering from cryptosporidiosis. J. Parasitol. 87, 90-95 (2001).
52. Gomez Morales MA, La Rosa G, Ludovisi A, Onori AM, Pozio E. Cytokine profile induced by Cryptosporidium antigen in peripheral blood mononuclear cells from immunocompetent and immunosuppressed persons with cryptosporidiosis. J. Infect. Dis. 179, 967-973 (1999).
53. White AC, Robinson P, Okhuysen PC et al. Interferon-γ expression in jejunal biopsies in experimental human cryptosporidiosis correlates with prior sensitization and control of oocyst excretion. J. Infect. Dis. 181, 701-709 (2000).
54. Mead JR, You X. Susceptibility differences to Cryptosporidium parvum infection in two strains of -γ interferon knockout mice. J. Parasitol. 84, 1045-1048 (1998).
55. Jakobi V, Petry F. Humoral immune response in IL-12 and IFN-γ deficient mice after infection with Cryptosporidium parvum. Parasite Immunol. 30, 151-161 (2008).
56. +a b+IL-4+ lymphocytes in gut-associated lymphoid tissue during resolution of infection. J. Immunol. 161, 1891-1900 (1998).
57. Tessema TS, Dauber E, Petry F. Adoptive transfer of protective immunity from Cryptosporidium parvum-infected interferon-γ and interleukin-12- deficient mice to naive recipients. Vaccine 27, 6575-6581 (2009).
58. McDonald SA, O'Grady JE, Bajaj-Elliott M et al. Protection against the early acute phase of Cryptosporidium parvum infection conferred by interleukin-4-induced expression of T helper 1 cytokines. J. Infect. Dis. 190, 1019-1025 (2004).
59. Urban JF Jr, Fayer R, Chen SJ, Gause WC, Gately MK, Finkelman FD. IL-12 protects immunocompetent and immunodeficient neonatal mice against infection with Cryptosporidium parvum. J. Immunol. 156, 263-268 (1996).
60. Ehigiator HN, Romagnoli P, Borgelt K et al. Mucosal cytokine and antigen-specific responses to Cryptosporidium parvum in IL-12p40 KO mice. Parasite Immunol. 27, 17-28 (2005).
61. Ehigiator HN, McNair N, Mead JR. Cryptosporidium parvum: the contribution of Th1-inducing pathways to the resolution of infection in mice. Exp. Parasitol. 115, 107-113 (2007).
62. Tessema TS, Schwamb B, Lochner M, Forster I, Jakobi V, Petry F. Dynamics of gut mucosal and systemic Th1/Th2 cytokine responses in interferon-γ and interleukin-12p40 knockout mice during primary and challenge Cryptosporidium parvum infection. Immunobiology 214, 454-466 (2009).
63. Smith LM, Bonafonte MT, Campbell LD, Mead JR. Exogenous interleukin-12 (IL-12) exacerbates Cryptosporidium parvum infection in -γ interferon knockout mice. Exp. Parasitol. 98, 123-133 (2001).
64. Davami MH, Bancroft GJ, McDonald V. Cryptosporidium infection in major histocompatibility complex congeneic strains of mice: variation in susceptibility and the role of T-cell cytokine responses. Parasitol. Res. 83, 257-263 (1997).
65. + Th1- and Th2-cell-secreted cytokines in cryptosporidiosis. Folia Parasitol. (Praha) 40, 307-311 (1993).
66. Lacroix S, Mancassola R, Naciri M, Laurent F. Cryptosporidium parvum-specific mucosal immune response in C57BL/6 neonatal and -γ interferon-deficient mice: role of tumor necrosis factor a in protection. Infect. Immun. 69, 1635-1642 (2001).
67. Lean IS, McDonald SA, Bajaj-Elliott M, Pollok RC, Farthing MJ, McDonald V. Interleukin-4 and transforming growth factor b have opposing regulatory effects on -γ interferon-mediated inhibition of Cryptosporidium parvum reproduction. Infect. Immun. 71, 4580-4585 (2003).
68. Mead JR, Arrowood MJ, Sidwell RW, Healey MC. Chronic Cryptosporidium parvum infections in congenitally immunodeficient SCID and nude mice. J. Infect. Dis. 163, 1297-1304 (1991).
69. Chen W, Harp JA, Harmsen AG, Havell EA. -γ interferon functions in resistance to Cryptosporidium parvum infection in severe combined immunodeficient mice. Infect. Immun. 61, 3548-3551 (1993).
70. Hayward AR, Chmura K, Cosyns M. Interferon-γ is required for innate immunity to Cryptosporidium parvum in mice. J. Infect. Dis. 182, 1001-1004 (2000).
71. McDonald V, Smith R, Robinson H, Bancroft G. Host immune responses against Cryptosporidium. Contrib. Microbiol. 6, 75-91 (2000).
72. Takeuchi D, Jones VC, Kobayashi M, Suzuki F. Cooperative role of macrophages and neutrophils in host antiprotozoan resistance in mice acutely infected with Cryptosporidium parvum. Infect. Immun. 76, 3657-3663 (2008).
73. + T cells are not essential for control of early acute Cryptosporidium parvum infection in neonatal mice. Infect. Immun. 79, 1647-1653 (2011).
74. Mancassola R, Lacroix-Lamande S, Barrier M, Naciri M, Salmon H, Laurent F. Increased susceptibility of b7-integrin-deficient neonatal mice in the early stage of Cryptosporidium parvum infection. Infect. Immun. 72, 3634-3637 (2004).
75. Barakat FM, McDonald V, Foster GR, Tovey MG, Korbel DS. Cryptosporidium parvum infection rapidly induces a protective innate immune response involving type I interferon. J. Infect. Dis. 200, 1548-1555 (2009).
76. Zhao J, Kim KD, Yang X, Auh S, Fu YX, Tang H. Hyper innate responses in neonates lead to increased morbidity and mortality after infection. Proc. Natl Acad. Sci. USA 105, 7528-7533 (2008).
77. Rogers KA, Rogers AB, Leav BA et al. MyD88-dependent pathways mediate resistance to Cryptosporidium parvum infection in mice. Infect. Immun. 74, 549-556 (2006).
78. Barrier M, Lacroix-Lamande S, Mancassola R et al. Oral and intraperitoneal administration of phosphorothioate oligodeoxynucleotides leads to control of Cryptosporidium parvum infection in neonatal mice. J. Infect. Dis. 193, 1400-1407 (2006).
79. Ungar BL, Soave R, Fayer R, Nash TE. Enzyme immunoassay detection of immunoglobulin M and -γ antibodies to Cryptosporidium in immunocompetent and immunocompromised persons. J. Infect. Dis. 153, 570-578 (1986).
80. Peeters JE, Villacorta I, Vanopdenbosch E et al. Cryptosporidium parvum in calves: kinetics and immunoblot analysis of specific serum and local antibody responses (immunoglobulin A [IgA], IgG, and IgM) after natural and experimental infections. Infect. Immun. 60, 2309-2316 (1992).
81. Hill BD, Blewett DA, Dawson AM, Wright S. Analysis of the kinetics, isotype and specificity of serum and coproantibody in lambs infected with Cryptosporidium parvum. Res. Vet. Sci. 48, 76-81 (1990).
82. Priest JW, Bern C, Xiao L et al. Longitudinal analysis of cryptosporidium species-specific immunoglobulin -γ antibody responses in Peruvian children. Clin. Vaccine Immunol. 13, 123-131. (2006).
83. Cozon G, Biron F, Jeannin M, Cannella D, Revillard JP. Secretory IgA antibodies to Cryptosporidium parvum in AIDS patients with chronic cryptosporidiosis. J. Infect. Dis. 169, 696-699 (1994).
84. Frost FJ, Tollestrup K, Craun GF, Fairley CK, Sinclair MI, Kunde TR. Protective immunity associated with a strong serological response to a Cryptosporidium-specific antigen group, in HIV-infected individuals. J. Infect. Dis. 192, 618-621 (2005).
85. Albert MM, Rusnak J, Luther MF, Graybill JR. Treatment of murine cryptosporidiosis with anticryptosporidial immune rat bile. Am. J. Trop. Med. Hyg. 50, 112-119 (1994).
86. Enriquez FJ, Riggs MW. Role of immunoglobulin A monoclonal antibodies against P23 in controlling murine Cryptosporidium parvum infection. Infect. Immun. 66, 4469-4473 (1998).
87. Taghi-Kilani R, Sekla L, Hayglass KT. The role of humoral immunity in Cryptosporidium spp. infection. Studies with B cell-depleted mice. J. Immunol. 145, 1571-1576 (1990).
88. Chen W, Harp JA, Harmsen AG. Cryptosporidium parvum infection in gene-targeted B cell-deficient mice. J. Parasitol. 89, 391-393 (2003).
89. Tzipori S, Roberton D, Cooper DA, White L. Chronic cryptosporidial diarrhoea and hyperimmune cow colostrum. Lancet 2, 344-345 (1987).
90. Fayer R, Andrews C, Ungar BL, Blagburn B. Efficacy of hyperimmune bovine colostrum for prophylaxis of cryptosporidiosis in neonatal calves. J. Parasitol. 75, 393-397 (1989).
91. Fayer R, Perryman LE, Riggs MW. Hyperimmune bovine colostrum neutralizes Cryptosporidium sporozoites and protects mice against oocyst challenge. J. Parasitol. 75, 151-153 (1989).
92. Jenkins M, Kerr D, Fayer R, Wall R. Serum and colostrum antibody responses induced by jet-injection of sheep with DNA encoding a Cryptosporidium parvum antigen. Vaccine 13, 1658-1664 (1995).
93. Sagodira S, Buzoni-Gatel D, Iochmann S, Naciri M, Bout D. Protection of kids against Cryptosporidium parvum infection after immunization of dams with CP15-DNA. Vaccine 17, 2346-2355 (1999).
94. Okhuysen PC, Chappell CL, Crabb J, Valdez LM, Douglass ET, DuPont HL. Prophylactic effect of bovine anti- Cryptosporidium hyperimmune colostrum immunoglobulin in healthy volunteers challenged with Cryptosporidium parvum. Clin. Infect. Dis. 26, 1324-1329 (1998).
95. Schaefer DA, Auerbach-Dixon BA, Riggs MW. Characterization and formulation of multiple epitope-specific neutralizing monoclonal antibodies for passive immunization against cryptosporidiosis. Infect. Immun. 68, 2608-2616 (2000).
96. McDonald V, Shirley MW. Past and future: vaccination against Eimeria. Parasitology 136, 1477-1489 (2009).
97. Jenkins M, Higgins J, Kniel K, Trout J, Fayer R. Protection of calves against cryptosporiosis by oral inoculation with g-irradiated Cryptosporidium parvum oocysts. J. Parasitol. 90, 1178-1180 (2004).
98. Boulter-Bitzer JI, Lee H, Trevors JT. Molecular targets for detection and immunotherapy in Cryptosporidium parvum. Biotechnol. Adv. 25, 13-44 (2007).
99. Ehigiator HN, Romagnoli P, Priest JW, Secor WE, Mead JR. Induction of murine immune responses by DNA encoding a 23-kDa antigen of Cryptosporidium parvum. Parasitol. Res. 101, 943-950 (2007).
100. Zheng J, Ren W, Pan Q et al. A recombinant DNA vaccine encoding Cryptosporidium andersoni oocyst wall protein induces immunity against experimental C. parvum infection. Vet. Parasitol. 179, 7-13 (2011).
101. Pasetti MF, Simon JK, Sztein MB, Levine MM. Immunology of gut mucosal vaccines. Immun. Rev. 239, 125-148 (2011).
102. Hammerschmidt SI, Friedrichsen M, Boelter J et al. Retinoic acid induces homing of protective T and B cells to the gut after subcutaneous immunization in mice. J. Clin. Invest. 121(8), 3051-3061 (2011).
103. Gooi HC. Gastrointestinal and liver involvement in primary immunodeficiency. In: Gastrointestinal and Hepatic Immunology. Healey HV (Ed.). Cambridge University Press, Cambridge, UK, 169-177 (1994).
104. Ungar BL, Ward DJ, Fayer R, Quinn CA. Cessation of Cryptosporidium- associated diarrhea in an acquired immunodeficiency syndrome patient after treatment with hyperimmune bovine colostrum. Gastroenterology 98, 486-489 (1990).
105. Xu P, Widmer G, Wang Y et al. The genome of Cryptosporidium hominis. Nature 431, 1107-1112 (2004).